Divergent cis-regulatory evolution underlies the convergent loss of sodium channel expression in electric fish

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Abstract

South American and African weakly electric fish independently evolved electric organs from muscle. In both groups, a voltage-gated sodium channel gene independently lost expression from muscle and gained it in the electric organ, allowing the channel to become specialized for generating electric signals. It is unknown how this voltage-gated sodium channel gene is targeted to muscle in any vertebrate. We describe an enhancer that selectively targets sodium channel expression to muscle. Next, we demonstrate how the loss of this enhancer, but not trans-activating factors, drove the loss of sodium channel gene expression from muscle in South American electric fish. While this enhancer is also altered in African electric fish, key transcription factor binding sites and enhancer activity are retained, suggesting that the convergent loss of sodium channel expression from muscle in these two electric fish lineages occurred via different processes.

Abstract

Solving the mystery of how a gene is exclusively expressed in muscle elucidates the evolution of electric organs in fishes.

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Most cited references 35

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The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs.

Kristen Kwan, Esther Fujimoto, Clemens Grabher … (2007)

Transgenesis is an important tool for assessing gene function. In zebrafish, transgenesis has suffered from three problems: the labor of building complex expression constructs using conventional subcloning; low transgenesis efficiency, leading to mosaicism in transient transgenics and infrequent germline incorporation; and difficulty in identifying germline integrations unless using a fluorescent marker transgene. The Tol2kit system uses site-specific recombination-based cloning (multisite Gateway technology) to allow quick, modular assembly of [promoter]-[coding sequence]-[3' tag] constructs in a Tol2 transposon backbone. It includes a destination vector with a cmlc2:EGFP (enhanced green fluorescent protein) transgenesis marker and a variety of widely useful entry clones, including hsp70 and beta-actin promoters; cytoplasmic, nuclear, and membrane-localized fluorescent proteins; and internal ribosome entry sequence-driven EGFP cassettes for bicistronic expression. The Tol2kit greatly facilitates zebrafish transgenesis, simplifies the sharing of clones, and enables large-scale projects testing the functions of libraries of regulatory or coding sequences. Copyright 2007 Wiley-Liss, Inc.

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Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life

Dahiana Arcila, Guillermo Ortí, Richard P. Vari … (2017)

Much progress has been achieved in disentangling evolutionary relationships among species in the tree of life, but some taxonomic groups remain difficult to resolve despite increasing availability of genome-scale data sets. Here we present a practical approach to studying ancient divergences in the face of high levels of conflict, based on explicit gene genealogy interrogation (GGI). We show its efficacy in resolving the controversial relationships within the largest freshwater fish radiation (Otophysi) based on newly generated DNA sequences for 1,051 loci from 225 species. Initial results using a suite of standard methodologies revealed conflicting phylogenetic signal, which supports ten alternative evolutionary histories among early otophysan lineages. By contrast, GGI revealed that the vast majority of gene genealogies supports a single tree topology grounded on morphology that was not obtained by previous molecular studies. We also reanalysed published data sets for exemplary groups with recalcitrant resolution to assess the power of this approach. GGI supports the notion that ctenophores are the earliest-branching animal lineage, and adds insight into relationships within clades of yeasts, birds and mammals. GGI opens up a promising avenue to account for incompatible signals in large data sets and to discern between estimation error and actual biological conflict explaining gene tree discordance.

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Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene.

P Hasty, A. Bradley, J H Morris … (1993)

Myogenin is a muscle-specific transcription factor that can induce myogenesis in a variety of cell types in tissue culture. To test myogenin's role in vivo, mice homozygous for a targeted mutation in the myogenin gene were generated. These mice survive fetal development but die immediately after birth and show a severe reduction of all skeletal muscle. Myogenin-mutant mice differ from mice carrying mutations in genes for the related myogenic factors Myf5 and MyoD, which have no muscle defects. Myogenin is therefore essential for the development of functional skeletal muscle.

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Author and article information

Contributors

Sarah LaPotin:

ORCID: https://orcid.org/0000-0003-4778-4554

Role: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing - review & editing

Mary E. Swartz:

ORCID: https://orcid.org/0000-0002-7601-0147

Role: Data curationRole: InvestigationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - review & editing

David M. Luecke:

ORCID: https://orcid.org/0000-0001-5309-9153

Role: InvestigationRole: Visualization

Savvas J. Constantinou:

ORCID: https://orcid.org/0000-0002-7774-0897

Role: Investigation

Jason R. Gallant:

ORCID: https://orcid.org/0000-0002-6528-090X

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Johann K. Eberhart:

ORCID: https://orcid.org/0000-0001-5258-2477

Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Harold H. Zakon:

ORCID: https://orcid.org/0000-0002-3700-4668

Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: June 2022

Publication date (Electronic, pub): 01 June 2022

Volume: 8

Issue: 22

Electronic Location Identifier: eabm2970

Affiliations

[1 ]Department of Neuroscience, The University of Texas, Austin, TX 78712, USA.

[2 ]Department of Molecular Biosciences, The University of Texas, Austin, TX 78712, USA.

[3 ]Department of Integrative Biology, Michigan State University, East Lansing, MI 48824, USA.

[4 ]Ecology, Evolution, and Behavior Program, Michigan State University, East Lansing, MI 48824, USA.

[5 ]Department of Integrative Biology, The University of Texas, Austin, TX 78712, USA.

Author notes

[* ]Corresponding author. Email: h.zakon@ 123456austin.utexas.edu

[†]

Present address: Department of Human Genetics, University of Utah, Salt Lake City, UT 84112-5330, USA.

Author information

Sarah LaPotin https://orcid.org/0000-0003-4778-4554

Mary E. Swartz https://orcid.org/0000-0002-7601-0147

David M. Luecke https://orcid.org/0000-0001-5309-9153

Savvas J. Constantinou https://orcid.org/0000-0002-7774-0897

Jason R. Gallant https://orcid.org/0000-0002-6528-090X

Johann K. Eberhart https://orcid.org/0000-0001-5258-2477

Harold H. Zakon https://orcid.org/0000-0002-3700-4668

Article

Publisher ID: abm2970

DOI: 10.1126/sciadv.abm2970

PMC ID: 9159570

PubMed ID: 35648851

SO-VID: 9af037ec-aa4c-49fc-b4ef-0ec501942d15

Copyright © Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

History

Date received : 07 September 2021

Date accepted : 13 April 2022

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;

Award ID: 1856695

Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;

Award ID: 1644965

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: R35DE029086

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: R01AA023426

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: 1856695

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: R35DE029086

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Divergent cis-regulatory evolution underlies the convergent loss of sodium channel expression in electric fish

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Behavioral Ecology of Fishes

Most cited references 35

The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs.

Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life

Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene.

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